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Abstract

Background

Laparoscopic liver surgery is becoming increasingly common. This cohort study was
designed to directly compare perioperative outcomes of the left lateral segmentectomy
via laparoscopic and open approach.

Methods

Between 2002 and 2006 43 left lateral segmentectomies were performed at King's College
Hospital. Those excluded from analysis included previous liver resections, polycystic
liver disease, liver cirrhosis and synchronous operations. Of 20 patients analysed,
laparoscopic (n = 10) were compared with open left lateral segmentectomy (n = 10).
Both groups had similar patient characteristics.

Results

Morbidity rates were similar with no wound or chest infection in either group. The
conversion rate was 10% (1/10). There was no difference in operating time between
the groups (median time 220 minutes versus 179 minutes, p = 0.315). Surgical margins
for all lesions were clear. Less postoperative opiate analgesics were required in
the laparoscopic group (median 2 days versus 5 days, p = 0.005). The median postoperative
in-hospital stay was less in the laparoscopic group (6 days vs 9 days, p = 0.005).
There was no mortality.

Conclusion

Laparoscopic left lateral segmentectomy is safe and feasible. Laparoscopic patients
may benefit from requiring less postoperative opiate analgesia and a shorter post-operative
in-hospital stay.

Background

Laparoscopic liver surgery, first performed in 1992 [1], is becoming the method of choice as surgical expertise in advanced laparoscopic
techniques has developed. Laparoscopic enthusiasts have shown that it is safe and
feasible to perform laparoscopic liver surgery [2-5]. Due to its anatomical accessibility left lateral segmentectomy (LLS) has been considered
the training operation for all liver surgeons [6].

Proposed benefits of laparoscopic liver surgery include reduced overall blood loss,
shorter hospital stay and less post-operative pain with a faster return to normal
activity. But there are concerns as reported complications have included compromised
oncological integrity [7-11], uncontrollable bleeding [10,12,13] and gas emboli [14-17].

To date one study has compared laparoscopic left lateral segmentectomy with an open
approach using historical case controls [18]. Findings confirmed that the laparoscopic approach was safe and feasible, yet had
significantly longer operating times and no difference in post-operative in-patient
stay. The aim of this study was to undertake a contemporaneous comparison between
laparoscopic and open left lateral segmentectomies.

Methods

We undertook a retrospective cohort study of the left lateral segmentectomies in our
institution between July 2002 and October 2006 (n = 43). Cases were included on an
intention to treat basis however, in an attempt to reduce bias, patients having previous
liver resections (n = 2), synchronous operations (n = 14), polycystic liver disease
(n = 3), liver cirrhosis (n = 3) and hand port assisted procedure (n = 1) were excluded
(see figure 1). This resulted in 20 left lateral segmentectomies for comparison, 10 in the laparoscopic
(LG) and 10 in the open group (OG). Selection was based on referral to the individual
consultants with all laparoscopic operations performed by a single surgeon (AGP) and
open operations under the care of two surgeons (NH, MR). Selection-bias was minimised
by the random referral policy to the individual surgeons over this time period. All
cases were discussed at the liver multi-disciplinary meeting pre-operatively. A detailed
review of the medical records was conducted. Data collection included patient characteristics,
site of lesion, operative details, postoperative analgesic requirements, morbidity
and mortality, postoperative in-hospital stay, pathology of specimen, weight of resected
specimen and tumour clearance margins. Ethical approval was not required.

All patients were operated on in the supine position under general anaesthesia with
endo-tracheal intubation. A broad spectrum antibiotic (Tazocin, Wyeth Laboratories,
Madison NJ) was given to all patients. Prophylaxis against deep vein thrombosis was
given in the form of low-molecular weight heparin, thrombo-embolic deterrent stockings
and intra-operative intermittent pneumatic compression boots. Staging laparoscopy
with intra-operative ultrasound was performed to exclude peritoneal disease and to
identify any additional tumours, as appropriate.

Laparoscopic technique

With the surgeon standing to the right of the patient pneumoperitoneum was established
after accessing the abdominal cavity using an open Hasson technique.

The initial port location varied depending upon previous surgery. Intra-abdominal
pressure was kept at approximately 15 mmHg. Four additional ports were inserted (figure
2). A 30° laparoscope was used. The falciform and left triangular ligament was divided
using a harmonic scalpel (Ethicon, Endo-Surgery Inc. Cincinnati Ohio). The falciform
ligament was used to retract and manipulate the left lobe of the liver.

Figure 2.Trocar placement for laparoscopic left lateral segmentectomy. For extraction a pfannenstiel incision is usually used.

The line of resection was marked using the diathermy hook, 5 mm left of the falciform
ligament and transected using a harmonic scalpel. In the umbilical fissure to the
left of the falciform ligament the segment II/III pedicles were stapled and divided
using Endo-GIA, 30 mm vascular staples (US Surgical, Norwalk CT). Liver parenchyma
was transected using a harmonic scalpel +/- .Cavitron Ultrasonic Surgical Aspirator
(CUSA®, Valleylab, Boulder CO). The left hepatic vein was approached intra-parenchymally
and transected with Endo-GIA 30 mm vascular staples. The final attachment to the left
triangular ligament close to the diaphragm was divided using hook diathermy and the
specimen freed. Specimens were removed using a retrieval bag through a pfannenstiel
or low midline incision. Fibrin glue was applied to the surface of the liver if required
and a closed suction drain was placed near the transected liver. The skin was closed
after infiltration of local anaesthetic (0.5% bupivacaine).

Open technique

The open left lateral segmentectomies were performed as described by Bismuth [19].

A laparotomy was performed via a transverse subcostal incision with a midline extension
if required. The left lobe of the liver was mobilised and the parenchyma was transected
using CUSA® and argon beam coagulation. With full mobilisation of the left lobe of the liver,
the segment II/III pedicles were ligated and divided. The left hepatic vein was clamped
at the end of the parenchymal transection and sutured with 5/0 prolene. Transection
occurred through the liver parenchyma using CUSA® and argon. Haemostasis was assured with the use of fibrin glue, and a drain was inserted.

Data Analysis

Statistical analysis was performed using Mann-Whitney U test unless otherwise stated. P-values < 0.05 were considered to be statistically
significant. All data is reported as median (range).

Results

Of the 43 liver resections performed in our institution between July 2002 and October
2006, 20 patients met the inclusion criteria for this study with 10 laparoscopic and
10 open left lateral segmentectomies. Patients presented with either solid lesions,
symptomatic liver cysts or liver abscesses, within segments II/III.

There were no differences in the patient characteristics between the two groups (Table
1). Median patient age was 54 years (25 - 72). 50% of patients were men (n = 10). The
patients had similar American Society of Anaesthesiology (ASA) grading (I:II:III);
1:5:4 in the laparoscopic group and 2:6:2 in the open group. Indication for left lateral
segmentectomy was malignant lesions in 50% of cases (n = 10).

Two patients in each group (20%) developed early complications (< 30 days postoperatively).
Minor morbidity in the laparoscopic group (LG) included one urinary tract infection,
and a haematemesis (possibly secondary to non-steroidal anti-inflammatory drugs) which
settled conservatively. In the open group (OG) one patient developed supraventricular
tachycardia four days post-operatively, exacerbated by low potassium levels, which
resolved spontaneously. The second patient developed hypoxia due to atelectasis, pleural
effusions and a superficial haematoma. Only one late complication occurred, a small
incisional hernia at the junction of the Mercedes incision in the OG 17 months postoperatively.
No statistically significant difference in morbidity between the two groups was found
(p = 0.725). There was no surgical mortality in either group.

In the laparoscopic group one conversion to open (10%) was necessary and occurred
early in the series. The LLS was performed for a liver tumour that showed evidence
of recent bleeding on a computerised tomography (CT) scan. Intra-operatively the tumour/haematoma
from the left lateral segment was found adherent to the greater curve of the stomach,
which required a wedge resection of the stomach. In order to avoid narrowing of the
oesophago-gastric junction the procedure was completed via an open approach.

Portal triad clamping was not used in the laparoscopic approach. In the OG it was
used intermittently in 50% (5/10) of patients, consultant preference. The median cumulative
clamp time duration was 35 minutes (20-60). There was no significant difference in
post-operative AST changes between the LG, OG (portal triad clamping) and OG (no portal
triad clamping), one-way ANOVA. Within the LG one patient required an intra-operative
blood transfusion (3 units) whilst in the OG two patients, both with liver abscesses,
required a transfusion (1-2 units). There was no statistical difference in intra-operative
blood transfusion requirement between the two groups (p = 0.782).

The median operating time for the LG was 220 minutes (116-335 minutes) versus 179
minutes (118-229 minutes) for the OG. No statistically significant difference was
found between the two groups, p = 0.315 (see Table 2). The laparoscopic operating time has reduced over the study period with median operating
time of 240 minutes in 2002, reduced to 163 minutes in 2006.

The LG had less analgesic requirements than the OG. This was exemplified by the statistically
significant median postoperative opiate use 2 days (1-5) in LG versus 5 days (2-14)
in the OG (p = 0.005).

Within the LG 80% (n = 8) of patients required one night in level II care. In the
OG 100% of the patients spent one night in level II care (p = 0.282), with one patient
requiring 4 nights of level II care. This patient was admitted as an emergency with
a liver abscess in the left lateral segment of the liver. The prolonged level II care
stay was due to multiple factors: poor post-operative analgesic control (unilateral
epidural block); ischaemic changes on ECG (Troponin I negative) and a hypoxic episode
day 2 post-operatively. A subsequent CT pulmonary angiogram revealed no pulmonary
emboli.

The median postoperative in-hospital stay for the LG was 6 days (2-7) compared to
9 days (6-14) for the OG, showing a highly significant difference, p = 0.005 (see
Table 2).

Histology is shown in Table 3. 60% (n = 6) of lesions in the LG and 40% (n = 4) in the open group were malignant.
The median total weight for the resected specimens in the LG was 243.5 g (99 g-577
g) versus 439 g (213 g-1480 g) in the OG (p = 0.023). Resection margins for all malignant
lesions were clear. In the LG the median resection margin was 15 mm (3-30 mm) with
the median in the OG 14.5 mm (< 1 mm ->20 mm)(p = 0.669).

The median follow-up in the LG was 18 months (0-63) and 6 months (0-33) in the OG.
Of the malignant cases, post-LLS recurrence in the liver has occurred in 2/6 of the
LG (median 14 months) and in 2/4 of the OG (19 months [10-28]). To date no port-site metastases have occurred in these patients.

Discussion

This study echoes the growing body of evidence demonstrating that a laparoscopic approach
to liver surgery provides tangible benefits to both patient and hospital. As surgical
skill develops it is anticipated that left lateral segmentectomy will shift from being
a traditionally open procedure to a laparoscopic one. This in turn may benefit an
increasing number of patients for whom open surgery could be considered high risk.

The findings of this study are consistent with other published series showing laparoscopic
liver surgery to be feasible and safe [2-5,12,20]. A 20% post-operative morbidity rate (< 30 days) was comparable between the open
and laparoscopic group. There were no liver related complications, chest or wound
infections in either group.

Within the laparoscopic group, conversion to an open procedure occurred in one patient
(10%) to ensure narrowing of the oesophago-gastric junction did not occur. The need
to convert to an open procedure has commonly resulted from uncontrollable bleeding
[12,13,18,20]. As surgical techniques improve conversion rates have decreased, with early experiences
reporting a 33% conversion rate [13] to Chang et al [20] reporting a 2.7% conversion rate due to bleeding. In this series no operations were
converted to open due to bleeding.

During design of this study we excluded cases in both groups which had undergone previous
liver resections, synchronous operations (liver resections, biliary procedures, reversal
of ileostomy, hernia repairs), polycystic liver disease (inc. fenestration of liver
cysts), liver cirrhosis and hand-port assisted procedures. The main objectives of
this study were to compare operative time, analgesic requirement and morbidity between
the open and laparoscopic approach. As such we felt it necessary to control for these
variables despite its impact on sample size. This is a retrospective cohort study
and as such we recognise the slight disparity in heterogeneity of pathologies included
in the final analysis.

Portal clamping was not required in the LG. In the OG 50% (n = 5) of patients underwent
clamping for a median duration of 35 mins (11-60 mins). Early experiences in the literature
utilised portal clamping to a greater extent with the laparoscopic versus the open
approach[18], with a resultant decrease in blood loss. In this series, the open group maintained
a low central venous pressure (CVP) and utilised intermittent portal clamping resulting
in minimal need for blood transfusion (20% n = 2). Whilst not requiring portal clamping,
the laparoscopic technique relied on the positive pressure of the pneumoperitoneum,
which in turn minimised potential blood loss, with only one patient (10%) receiving
a blood transfusion.

In laparoscopic liver surgery there are long standing concerns regarding gas emboli
[14] with laparoscopic surgeons opting for abdominal wall lifting (gasless laparoscopy)
or using low CO2 pressures to maintain pneumoperitoneum, to minimise any potential risk. Animal studies
have shown an increased risk of cardiac arrhythmias [15] and gas emboli in those with 16 mmHg compared to 8 mmHg (after the left hepatic vein
was left open for 3 minutes) [16]. Whilst this implies increased pneumoperitoneal pressures may exacerbate the risk
of gas emboli, no human data exists. Potential advantages of increased pneumoperitoneal
pressure include reduction in blood loss and improved visualisation of the operative
field. In this series pneumoperitoneal pressures were maintained at 15-20 mmHg with
no clinical adverse incidents however, a prospective study in this field is overdue.

No significant difference was found in the operating time between the two groups (220
vs 179 minutes, p = 0.315), consistent with both Mala et al [21] and Mamada et al [22]. Other groups have shown longer operating times in the LG [18,23]. Of interest, in the LG and the OG the shortest operating times were comparable (116
vs 118 minutes). It must be highlighted that the left lateral segmentectomy is considered
a training operation. As such, surgeons in training (under the supervision of the
Consultant) operated on some of the open group (n = 4). These data also includes the
first laparoscopic LLS performed by the laparoscopic surgeon therefore reflecting
the learning curve; the median laparoscopic operating time in 2002 was 240 minutes
and by 2006 it was 163 minutes. It is expected that laparoscopic operating time for
this procedure will continue to reduce however, these factors may affect comparison
of operative time.

One patient in the LG had an epidural (10%), while 90% (n = 9) required an epidural
in the OG (p = 0.003). It is not routine for the laparoscopic liver patients to require
epidural anaesthesia but is protocol for open liver resections to have an epidural
inserted preoperatively. In the LG, port-site infiltration of local anaesthetic was
used to optimise post-operative analgesia however, port-site infiltration has been
shown to have no impact on post-operative pain after analgesia [24]. To account for these discrepancies, we assessed the total number of days post-operative
opiate analgesia was required, including all methods of opiate administration. This
revealed significantly less opiate analgesia was required in the LG postoperatively
(2 vs 5 days, p = 0.005). In their randomised clinical trial Veldkamp et al [25] found there was a need for fewer analgesics in the laparoscopic vs open group following
surgery for colon cancer. This reduced demand for post-operative analgesia was also
found by Farges et al [26] with 50% less morphine (15.5 mg vs 31.6 mg) administered in the laparoscopic versus
open approach following liver resection.

All patients in the OG and 80% of the LG were routinely transferred to level II care
with a median stay of one night. With increased confidence and experience this policy
has since been modified. Currently patients from both groups no longer routinely require
level II care, and the more stringent use of these resources has favourable cost implications
for future service development.

In this study the median post-operative in-hospital stay was significantly less in
the LG than OG (6 vs 9 days, p = 0.005). In other comparative studies, laparoscopic
versus open liver resections for colorectal metastases the median post-operative stay
was 4 days vs 8.5 days (p < 0.001) [13], and for hepatic resections 7.8 days vs 11.6 days (p < 0.05) [23] and 10.4 vs 18.0 days (p < 0.05) [21]. This demonstrates reduced post-operative in-patient stay is a reproducible, safe
benefit of laparoscopic liver resection.

The weights of the resected specimens in the LG were significantly lower than the
OG (p = 0.023). On histological examination of the normal liver in the specimens there
was no difference with respect to clamping to account for the weight disparity. Mala
et al [21] also noted significantly lighter specimens resected laparoscopically, along with
no significant difference in resection margin involvement. This may reflect a slight
difference in operative techniques between the two approaches. The left hepatic vein
is approached and transection of the major vessels occurs intra-hepatically in the
laparoscopic group. We speculate that this results in a rounded superior resection,
accounting for this difference.

Oncological integrity is often questioned in laparoscopic liver resections for malignancy.
In this study resection margins were clear in all malignant cases (median laparoscopic
15 mm vs open 14.5 mm). However, early experiences of laparoscopic oncological surgery
resulted in an increased fear of developing abdominal wall metastases after laparoscopy
for hepatic cancer compared with open surgery. Hypotheses suggested the peritoneum
may be damaged by the pneumoperitoneum, inducing intra-peritoneal tumour growth [11]. However this notion is becoming outdated. A short-term animal study by Agnosti et
al [27] showed no significant difference in terms of tumour growth, irrespective of gas or
pneumoperitoneum pressure used. Jacobi et al [28] suggest intra-peritoneal tumour growth increases for pressures < 10 mmHg and decreases
at higher pressures. There is also further evidence that reported tumour growth in
colonic cancer was significantly reduced after CO2 laparoscopy when compared to gasless laparoscopy [29]. A meta-analysis of over 1 500 patients undergoing laparoscopic vs open colectomy
for colon cancer found no difference in the 3 year survival rate (82.2% vs 83.3%)
[30], concluding that a laparoscopic approach is indeed oncologically safe.

Any potential risk of port-site metastases can be reduced by maintaining an intact
surgical specimen and using plastic retrieval devices [20,31], thus minimising contact with the extra-peritoneal structures.

There is evidence that the reduced stress response of laparoscopic surgery may be
preferential in the malignant cases due to associated lower rates of infection and
potential reduction in tumour recurrence [32,33]. Animal data suggests that increased surgical stress augments cancer metastasis via
surgical stress-induced expression of proteinases in the target organ of metastasis
[34]. There is also a diminished stress response to the laparoscopic approach versus open
liver resection, preserving immune function [32].

An additional benefit of the laparoscopic approach is reduced adhesion formation [32] which may facilitate further liver resections for metastases. With an increasing
trend for non-anatomical and segmental resections with increased parenchymal preservation
[35], repeat metastectomies (and re-resections) are becoming more common. Petrowsky et
al [36] report similar outcomes for patients having either a primary or repeat laparoscopic
resection following an initial resection performed laparoscopically. These findings
have led to an increased number of patients undergoing further liver metastatectomy,
presenting a further interventional option as multiple staged liver resections become
more commonplace.

Conclusion

The laparoscopic approach to left lateral segmentectomy is safe and feasible with
reproducible results. In a specialised unit, it may offer no difference in operating
time, morbidity and mortality rates and oncological clearance. Potential benefits
include reduced opiate analgesic requirements and shorter hospital stay however, the
importance of patient selection cannot be over-emphasised.

Completing interests

The authors declare that they have no completing interests.

Authors' contributions

KC conceived of the study, participated in its design, data collection and analysis
and drafted the manuscript. FS participated in its design, data analysis and drafting
of the manuscript. BM assisted with data collection and drafting of the manuscript.
MR and NH participated in study design, carried out some of the operative procedures,
assisted with data collection and manuscript revisions. AGP participated in study
design and coordination, carried out the laparoscopic procedures, assisted with data
collection and supervised manuscript revisions.

All authors read and approved the final manuscript.

Acknowledgements

This paper has been presented in part to the Association of Surgeons of Great Britain
and Ireland, Edinburgh, UK, May 2006, published in abstract form as BJS 2006; 93(S1):
58, and presented to the 10th World Congress of Endoscopic Surgeons and European Association of Endoscopic Surgeons,
Berlin, Germany, September 2006, and published in abstract form as Surg Endosc 2007;
21: S64